Bull Environ Contam Toxicol DOI 10.1007/s00128-014-1448-6

Total and Monomethyl Mercury in Terrestrial from the Central California Coast

Cruz Ortiz Jr. • Peter S. Weiss-Penzias • Susanne Fork • A. Russell Flegal

Received: 17 July 2014 / Accepted: 19 December 2014 Ó Springer Science+Business Media New York 2014

Abstract The aim of this project was to obtain a baseline Keywords Atmospheric Mercury Terrestrial understanding and investigate the concentration of mercury Bioaccumulation Invertebrates (Hg) in the tissue of terrestrial arthropods. The 4-month sampling campaign took place around Monterey Bay, Cali- fornia. Total mercury (HgT) concentrations (x ± SD, dry The novelty, scientific significance, and importance weight) for the captured specimens ranged from 22 to of the Article 188 ng g-1 in the Jerusalem crickets (: Stenopel- matidae); 65–233 ng g-1 in the camel crickets (Orthoptera: The novelty and the importance of this study is that it’s ); 25–227 ng g-1 in the pill bugs (Isopoda: creating a baseline understanding of mercury cycling in Armadillidiidae); 19–563 ng g-1 in the ground terrestrial ecosystems. Unfortunately, there are very few (Coleoptera: Carabidae); 140–441 ng g-1 in the variegated other studies of mercury in terrestrial food chains meadowhawk dragonflies (Odonata: Libellulidae); for comparison. Hopefully this initial report will catalyze 607–657 ng g-1 in the pacific spiketail dragonflies (Odonata: new studies on the role of atmospheric deposition in the Cordulegastridae); and 81–1,249 ng g-1 in the wolf spiders biogeochemical cycling of mercury in terrestrial ecosys- (Araneae: Lycosidae). A subset of samples analyzed for tems. Moreover, the role of arthropods on the bioaccu- monomethyl mercury (MMHg) suggest detrital pill bugs have mulation and biomagnification of mercury in terrestrial a higher MMHg/HgT ratio than predatory ground beetles. food chains. Lastly, this investigation falls within BECT’s aims and scope because it characterizes variations of mercury contamination. The motivation for this study came from an investigation which received significant press- C. Ortiz Jr. P. S. Weiss-Penzias A. R. Flegal coverage in 2012–2013 \http://green.blogs.nytimes.com/ Institute of Marine Science, University of California - Santa 2012/03/28/coastal-california-fog-carries-toxic-mercury- Cruz, 1156 High Street, Santa Cruz, CA 95064, USA study-finds/[. e-mail: [email protected] Historic and on-going mercury contamination is of A. R. Flegal increasing concern for environmental and human health, as e-mail: fl[email protected] its toxic threshold continues to be lowered (Agency 2013; C. Ortiz Jr. (&) Organization 2010). That concern is based on the extensive Department of Environmental Engineering Sciences, bioaccumulation (factor of 107) of organic mercury to Engineering School of Sustainable Infrastructure and potentially toxic levels, especially in aquatic food chains Environment, University of Florida, 412 Black Hall, PO Box 116450, Gainesville, FL 32611-6450, USA (Fitzgerald et al. 2007; Scheulhammer et al. 2007). As a e-mail: cortiz@ufl.edu result, most research on the biomagnification of mercury has focused on aquatic environments. Arthropods are an S. Fork important source of protein for many organisms (Zhang Elkhorn Slough National Estuarine Research Reserve, PO Box 267, Moss Landing, CA 95039, USA et al. 2009); furthermore, a few recent studies have deter- e-mail: [email protected] mined that terrestrial food chains may be contaminated by 123 Bull Environ Contam Toxicol the cross-habitat transfer of mercury by and spiders arthropods: ground beetles (Coleoptera: Carabidae) (Brasso and Cristol 2008; Cristol et al. 2008; Henderson (n = 14), wolf spiders (Araneae: Lycosidae) (n = 58); et al. 2012). pacific spiketail dragonflies (Odonata: Cordulegastridae) Limited published data exist on Hg concentrations in (n = 2); and variegated meadowhawk dragonflies (Odo- terrestrial arthropods, and their potential as Hg pollution nata: Libellulidae) (n = 4). The adult dragonflies were bioindicators needs further investigation. Terrestrial captured with sweep nets, all the other arthropods were arthropods whose tissue is resistant to metallic pollutants captured using pit fall traps; these methods of collection are are often used as biological indicators for metal contami- described elsewhere (Chanthy et al. 2013; Greenslade nation in soil (Dallinger et al. 1992; Udovic et al. 2009). It 1964). Unbaited pitfall traps were deployed 2–4 consecu- is also recognized that flying arthropods such as mosqui- tive nights and checked within 24 h of deployment. toes may also be a useful indicator of atmospheric Hg The samples were placed in trace metal clean plastic contamination (Hammerschmidt and Fitzgerald 2005). containers, within a cooler, and then promptly transported Thus, the current study aimed to evaluate the efficacy of to UCSC. There they were rinsed with high purity using arthropods as indicators of Hg accumulation by (18.2 MX cm) water (Milli-QÒ) to remove surface con- measuring the concentration of Hg in the tissue of terres- taminants. Then they were dried, placed in trace metal trial arthropods from the central California coast, an clean plastic containers, frozen, and lyophilized prior to environment well known for its persistent summer-time fog analysis. (Weiss-Penzias et al. 2012). Mercury analyses were made using established trace metal clean techniques. The organisms (29–249 mg) were weighed (±0.1 mg), pulverized, transferred to 100 mL Methods and Materials acid-cleaned volumetric flasks, and digested with

10–20 mL of H2SO4–HNO3, using the methodology Samples were collected, using trace metal clean techniques described elsewhere (Liang et al. 1994). HgT concentra- at 3 sites around Monterey Bay, California: (1) Elkhorn tions in digestates were then determined by cold vapor Slough Estuarine Reserve (2) the University of California, atomic fluorescence spectrometry (CVAFS) with estab- Santa Cruz (UCSC), and (3) Chalk Mountain in An˜o Nu- lished methods that quantitatively measure Hg in aqueous evo State Park (Fig. 1). The 4-month arthropod sampling samples (Bloom and Fitzgerald 1988; Fitzgerald and Gill campaign took place between March and October of 2012. 1979). MMHg concentrations of six samples were then The samples included detrital arthropods: Jerusalem measured by CVAFS after distillation, aqueous ethylation, crickets (Orthoptera: ) (n = 7), camel purge and trap (Liang et al. 1994). The accuracy of the HgT crickets (Orthoptera: Rhaphidophoridae) (n = 11), and pill measurements was determined from concurrent analyses of bugs (Isopoda: Armadillidiidae) (n = 41); and predatory (1) procedural blanks, (2) Hg0 calibration standards, (3)

Fig. 1 Map of study location, Monterey Bay, California with sample sites at Elkhorn Slough Reserve (36°49012.700N, 121°44010.700W), the University of California, Santa Cruz (36°59028.500N, 122°03040.700W), and Chalk Mountain in An˜o Nuevo State Park (37°09037.900N, 122°17024.800W)

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National Research Council of Canada Certified Reference arthropods delineated in this study. There was notable tem- Material (CRM) DORM-2 (dogfish muscle), (4) replicate poral differences, although not statistically different aliquots from sample digests, and (5) replicate subsamples (p B 0.05), in HgT concentrations of some of the arthropods of arthropod digests from the parent samples. Three or in our study (Table 2). Although these comparisons might be more standard solutions were made for each analysis. All an artifact of a small sample size, they warrant further inves- analyses had standard regressions with simple linear cor- tigation. Total mercury concentrations in wolf spider had relation coefficients (R2) greater than 0.998. The HgT relatively comparable HgT concentrations in March procedural blank ranged between 11 and 25 parts per tril- (255 ± 97 ng g-1,n= 28), July (278 ± 127 ng g-1, lion (ppt), and the HgT concentration of the CRM (DORM- n = 5, and October (327 ± 173 ng g-1,n= 20), but those 2) ranged between 98 and 102 % of its certified value average concentrations were all less than half of the average (4.64 ± 0.26 lgg-1). HgT concentration of wolf spiders in August (846 ± 312 ng g-1,n= 5). The temporal difference coin- cided with the seasonal peak of fog that substantially increases Results and Discussion the flux of MMHg in the study site. A similar, albeit much smaller, seasonal increase was also observed in camel crick- There is a lack of published values in the literature for ets, but not pill bugs (Fig. 2). Fog data reported for 2012 was comparison; furthermore, the values published have a very obtained from Monterey Regional Airport (MRY); mean daily high variance, as is the case with this study. HgT con- visibility below 15.5 km is the threshold for reported fog centrations (x ± SD, dry weight) of the 134 insects and occurrences at MRY and is indicative of a foggy day. spiders measured in this study, along with HgT values The positive covariance of high HgT concentrations in previously reported for some of those organisms (Cristol wolf spiders, and to a much lesser extent in camel crickets, et al. 2008; Rimmer et al. 2010; Zhang et al. 2009) are does not seem to correspond with any known variables. listed in Table 1. There is no statistically difference Since the life span of male wolf spiders is about a year, (p B 0.05, t test) in HgT concentrations among any of the with most adolescents in February through March (Punzo species measured at the different sites, those comparisons and Farmer 2006), HgT concentrations in the spiders are limited by the high variance of mercury values. For should have been highest in October if that uptake was example, the relative standard deviation (%) of HgT in simply due to temporal bioaccumulation. And since the spiders in our study was 73.6 ng g-1 (n = 58) and that in camel population is relatively constant over time, the study by Cristol et al. (2008) was 118.5 ng g-1 with no seasonal period of intense reproduction (Lavoie (n = 101). Due to this high variance, significant differ- et al. 2007), there does not appear to be a physiological ences in Hg concentration between sites could not be explanation for the corresponding maximum in the HgT established for any of the arthropods analyzed. concentrations during August in that coastal zone. Predatory wolf spiders had the highest concentrations of Although fog may be at question, at this time it cannot be HgT in this study, as is the case with two of the three compared determined because we know very little on how MMHg in studies, no other pattern was observed with the other groups of fog impacts terrestrial ecosystems.

Table 1 Mean HgT concentrations for this and other studies, all concentrations expressed in (x ± SD, ng g-1 dry weight) ID This study Zhang et al. (2009) Huludao, China Rimmer et al. (2010) Vermont, USA Cristol et al. (2008) Virginia, USA (n) Mean Range Mean (n) Mean

Spiders 58 401 ± 295 15–1,099 173 ± 81 101 1 240 ± 1 470 Camel Crickets 11 125 ± 62 12–866 10 ± 5 50 310 ± 1 220 Ground Beetles 14 134 ± 157 48 ± 67 Pill Bugs 41 124 ± 47 Jerusalem Crickets 7 109 ± 73 Spiketail 2 632 ± 25 Meadowhawk 4 220 ± 112 Dragonflies 6 338 ± 209 233–1,2 432 Moths–Butterflies 5 ± 7 137 380 ± 2,080

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Table 2 Total mercury (HgT) ID March July August October results, (n) represents number of samples analyzed, all (n) Mean (n) Mean (n) Mean (n) Mean concentrations expressed in (x ± SD, ng g-1 dry weight) Wolf Spiders 28 255 ± 97 5 278 ± 127 5 846 ± 312 20 327 ± 173 Camel Crickets 3 62 ± 33 2 139 ± 29 2 217 ± 17 4 120 ± 29 Ground beetles 11 67 ± 47 2 470 ± 93 1 193 0 N/A Pill Bugs 13 155 ± 29 13 107 ± 66 5 124 ± 13 10 151 ± 29 Jerusalem Cricket 2 20 ± 14 0 N/A 0 N/A 5 142 ± 53 Pacific Spiketail 0 N/A 0 N/A 2 634 ± 25 0 N/A Meadowhawk 0 N/A 0 N/A 0 N/A 4 220 ± 112

Fig. 2 2012 temporal variation 1400 26 of total mercury (HgT) concentrations and number of Wolf Spiders 24 1200 Camel Crickets foggy days Pill Bugs Fog 22 1000

dry wt.) 20 -1

800 18

600 16

14 400

12 Number of Foggy Days

Mean [HgT] ppb (ng g 200 10

0 8 March July August October Time (month)

The absence of a similar temporal peak in HgT con- Table 3 Monomethyl mercury (MMHg) Results for individual centrations of pill bugs may be due to many factors. One samples, all concentrations expressed in ng g-1 in dry weight possibility is that pill bugs may be resistant to trace-metal Location Common name [HgT] [MMHg] % MMHg contaminants in soil, as reported for some other arthropods (Dallinger et al. 1992; Udovic et al. 2009). Unfortunately, Elkhorn Slough Wolf Spider 389 294 76 the sample size during the four sampling periods was quite Santa Cruz Wolf Spider 332 252 76 small (n = 5–13) and there is no information on their Elkhorn Slough Pill bug 92 46 50 mercury toxicokinetics to address their relatively consistent Santa Cruz Pill bug 150 88 59 HgT concentrations. As primary consumers, Hg concen- Elkhorn Slough Ground 28 4 16 trations in pill bug tissue may reflect those in the ambient Santa Cruz Ground Beetle 189 28 15 environment as opposed to Hg resulting from food chain transfer; this may render them potential bioindicators of Hg pollution. MMHg concentrations and ratios of MMHg/HgT (% inorganic mercury is not readily bioaccumulated and bio- MMHg) measured in the 6 arthropod subsamples (2 pill magnified. Therefore, those lower ratios may be an artifact bugs, 2 ground beetles, and 2 wolf spiders) are listed in of inorganic mercury sorbed on the insects exoskeletons Table 3. While the MMHg analyses of the 3 types of and/or ingested sediments with relatively high amounts of arthropods was very small (n = 2), the variation in the % inorganic mercury compared to organic mercury. Pill bugs, MMHg was surprisingly limited. As expected, the highest detrital arthropods, feed on decaying matter and live most % MMHg was in predatory wolf spiders (76 %). The lower of their life below soil (Capinera 2010). One explanation ratios in pill bugs (50–59 %) and predatory ground beetles for the higher ratio found in pill bugs could be the uptake (15–16 %), especially the latter, were surprising because of MMHg provided by higher trophic level carrion; another

123 Bull Environ Contam Toxicol explanation could be their uptake of soil MMHg which has Caffrey JM, Hollibaugh JT, Bano N, Haskins J (2010) Effects of been synthesized by bacteria (Caffrey et al. 2010; Compeau upwelling on short-term variability in microbial and biogeo- chemical processes in estuarine sediments from Elkhorn Slough, and Bartha 1985; Kerin et al. 2006). Again, these and other California, USA. Aquat Microb Ecol 58:261–271. doi:10.3354/ factors cannot be assessed at this time because there is so ame01387 little information on mercury in terrestrial arthropod food Capinera JL (2010) Insects and wildlife: arthropods and their chains. relationships with wild vertebrate Insects and wildlife: arthropods and their relationships with wild vertebrate animals:i- Marine fog along the central California coastline has viii, 1–487 been shown to contain higher Hg concentrations and higher Chanthy P, Martin RJ, Gunning RV, Andrew NR (2013) Arthropod ratios of MMHg/HgT than those seen in coastal rainwater survey on soybean crops in Cambodia: a comparison of the (Weiss-Penzias et al. 2012); and fog is a major contributor sweep netting and beat sheeting collection methods for estimat- ing arthropod diversity and species richness. Aust J Entomol to the hydrologic cycle in California’s coastal redwood 52:299–308. doi:10.1111/aen.12035 forests in the summer months (Azevedo and Morgan 1974; Compeau GC, Bartha R (1985) Sulfate-reducing bacteria–principal Dawson 1998; Ingraham and Matthews 1995). This data methylators of mercury in anoxic estuarine sediment. Appl may partially substantiate a hypothesis that atmospheric Environ Microbiol 50:498–502 Dallinger R, Berger B, Birkel S (1992) Terrestrial isopods—useful deposition of mercury in coastal fog increases HgT in the biological indicators of urban metal pollution. Oecologia tissue of terrestrial arthropods, but there is still too little 89:32–41. doi:10.1007/bf00319012 information on the biological mechanism for the movement Dawson TE (1998) Fog in the California redwood forest: ecosystem of Hg in coastal fog to terrestrial habitats. inputs and use by plants. Oecologia 117:476–485. doi:10.1007/ s004420050683 In conclusion, the ratio of MMHg/HgT in pill bugs Fitzgerald WF, Gill GA (1979) Sub-nanogram determination of compared to that in ground beetles, and the covariance of mercury by 2-stage gold amalgamation and gas-phase detection HgT concentration in wolf spiders with the peak period of applied to atmospheric analysis. Anal Chem 51:1714–1720. marine fog deposition are both intriguing. Unfortunately, doi:10.1021/ac50047a030 Fitzgerald WF, Lamborg CH, Hammerschmidt CR (2007) Marine there are very few other studies of mercury in terrestrial biogeochemical cycling of mercury. Chem Rev 107:641–662. arthropod food chains for comparison. Hopefully this ini- doi:10.1021/cr050353m tial report will catalyze new studies on the role of atmo- Greenslade PJM (1964) Pitfall trapping as a method for studying spheric deposition in the biogeochemical cycling of populations of carabidae (Coleoptera). J Anim Ecol 33:301–310. doi:10.2307/2632 mercury in terrestrial ecosystems. Moreover, the role of Hammerschmidt CR, Fitzgerald WF (2005) Methylmercury in arthropods on the bioaccumulation and biomagnification of mosquitoes related to atmospheric mercury deposition and mercury in terrestrial food chains. contamination. Environ Sci Technol 39:3034–3039. doi:10. 1021/es0485107 Acknowledgments The authors would like to thank the Louis Henderson BL, Chumchal MM, Drenner RW, Deng Y, Diaz P, Stokes California Alliance for Minority Participation in STEM and Nowlin WH (2012) Effects of fish on mercury contamination of the University of California at Santa Cruz (UCSC) Friends of Long macroinvertebrate communities of Grassland ponds. Environ Marine Laboratory for their financial support; members of the WIGS Toxicol Chem 31:870–876. doi:10.1002/etc.1760 laboratory, especially Priya Ganguli, Christopher Conaway, and Ingraham NL, Matthews RA (1995) The importance of fog-drip water Robert Franks for their technical support; Christopher Lay, Jennifer to vegetation—point-reyes peninsula, California. J Hydrol Rojero and Paul Dvorson for their assistance in sampling; and lastly 164:269–285. doi:10.1016/0022-1694(94)02538-m the An˜o Nuevo State Park Rangers for facilitating the access to Chalk Kerin EJ, Gilmour CC, Roden E, Suzuki MT, Coates JD, Mason RP Mountain. (2006) Mercury methylation by dissimilatory iron-reducing bacteria. Appl Environ Microbiol 72:7919–7921. doi:10.1128/ aem.01602-06 Lavoie KH, Helf KL, Poulson TL (2007) The biology and ecology of North American cave crickets. 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